Avniel Singh Ghuman

Top-Down Predictions in the Cognitive Brain.

The human brain is not a passive organ simply waiting to be activated by external stimuli. Instead, we propose that the brain continuously employs memory of past experiences to interpret sensory information and predict the immediately relevant future. The basic elements of this proposal include analogical mapping, associative representations and the generation of predictions. This review concentrates on visual recognition as the model system for developing and testing ideas about the role and mechanisms of top-down predictions in the brain. We cover relevant behavioral, computational and neural aspects, explore links to emotion and action preparation, and consider clinical implications for schizophrenia and dyslexia. We then discuss the extension of the general principles of this proposal to other cognitive domains.

The effects of priming on frontal-temporal communication

Repeated exposure to a stimulus facilitates its processing. This is reflected in faster and more accurate identification, reduced perceptual identification thresholds, and more efficient classifications for repeated compared with novel items. Here, we test a hypothesis that this experience-based behavioral facilitation is a result of enhanced communication between distinct cortical regions, which reduces local processing demands. A magnetoencephalographic investigation revealed that repeated object classification led to decreased neural responses in the prefrontal cortex and temporal cortex. Critically, this decrease in absolute activity was accompanied by greater neural synchrony (a measure of functional connectivity) between these regions with repetition. Additionally, the onset of the enhanced interregional synchrony predicted the degree of behavioral facilitation. These findings suggest that object repetition results in enhanced interactions between brain regions, which facilitates performance and reduces processing demands on the regions involved.

Early onset of neural synchronization in the contextual associations network

Objects are more easily recognized in their typical context. However, is contextual information activated early enough to facilitate the perception of individual objects, or is contextual facilitation caused by postperceptual mechanisms? To elucidate this issue, we first need to study the temporal dynamics and neural interactions associated with contextual processing. Studies have shown that the contextual network consists of the parahippocampal, retrosplenial, and medial prefrontal cortices. We used functional MRI, magnetoencephalography, and phase synchrony analyses to compare the neural response to stimuli with strong or weak contextual associations. The context network was activated in functional MRI and preferentially synchronized in magnetoencephalography (MEG) for stimuli with strong contextual associations. Phase synchrony increased early (150–250 ms) only when it involved the parahippocampal cortex, whereas retrosplenial–medial prefrontal cortices synchrony was enhanced later (300–400 ms). These results describe the neural dynamics of context processing and suggest that context is activated early during object perception.

Face Adaptation Without a Face

Prolonged viewing of a stimulus results in a subsequent perceptual bias. This perceptual adaptation and the resulting aftereffect reveal important characteristics regarding how perceptual systems are tuned. These aftereffects occur not only for simple stimulus features but also for high-level stimulus properties. Here we report a novel cross-category adaptation aftereffect demonstrating that prolonged viewing of a human body without a face shifts the perceptual tuning curve for face gender and face identity. This contradicts a central assumption underlying perceptual adaptation: that adaptation depends on physical similarity between how the adapting and the adapted features are perceived. Additionally, this aftereffect was not due to response bias, because its dependence on adaptation duration resembled traditional perceptual aftereffects. These body-to-face adaptation results demonstrate that bodies alone can alter the tuning properties of neurons that code for the gender and identity of faces. More generally, these results reveal that high-level perceptual adaptation can occur when the property or features being adapted are automatically inferred rather than perceived in the adapting stimulus.

Dynamic encoding of face information in the human fusiform gyrus

Humans’ ability to rapidly and accurately detect, identify, and classify faces under variable conditions derives from a network of brain regions highly tuned to face information. The fusiform face area (FFA) is thought to be a computational hub for face processing, however temporal dynamics of face information processing in FFA remains unclear. Here we use multivariate pattern classification to decode the temporal dynamics of expression-invariant face information processing using electrodes placed directly upon FFA in humans. Early FFA activity (50-75 ms) contained information regarding whether participants were viewing a face. Activity between 200-500 ms contained expression-invariant information about which of 70 faces participants were viewing along with the individual differences in facial features and their configurations. Long-lasting (500+ ms) broadband gamma frequency activity predicted task performance. These results elucidate the dynamic computational role FFA plays in multiple face processing stages and indicate what information is used in performing these visual analyses.

Network Effects of Deep Brain Stimulation

The ability to differentially alter specific brain functions via deep brain stimulation (DBS) represents a monumental advance in clinical neuroscience, as well as within medicine as a whole. Despite the efficacy of DBS in the treatment of movement disorders, for which it is often the gold-standard therapy when medical management becomes inadequate, the mechanisms through which DBS in various brain targets produces therapeutic effects is still not well understood. This limited knowledge is a barrier to improving efficacy and reducing side effects in clinical brain stimulation. A field of study related to assessing the network effects of DBS is gradually emerging that promises to reveal aspects of the underlying pathophysiology of various brain disorders and their response to DBS that will be critical to advancing the field. This review summarizes the nascent literature related to network effects of DBS measured by cerebral blood flow and metabolic imaging, functional imaging, and electrophysiology (scalp and intracranial electroencephalography and magnetoencephalography) in order to establish a framework for future studies.

Cortical Neurodynamics of Inhibitory Control

The ability to inhibit prepotent responses is critical for successful goal-directed behaviors. To investigate the neural basis of inhibitory control, we conducted a magnetoencephalography study where human participants performed the antisaccade task. Results indicated that neural oscillations in the prefrontal cortex (PFC) showed significant task modulations in preparation to suppress saccades. Before successfully inhibiting a saccade, beta-band power (18–38 Hz) in the lateral PFC and alpha-band power (10–18 Hz) in the frontal eye field (FEF) increased. Trial-by-trial prestimulus FEF alpha-band power predicted successful saccadic inhibition. Further, inhibitory control enhanced cross-frequency amplitude coupling between PFC beta-band (18–38 Hz) activity and FEF alpha-band activity, and the coupling appeared to be initiated by the PFC. Our results suggest a generalized mechanism for top-down inhibitory control: prefrontal beta-band activity initiates alpha-band activity for functional inhibition of the effector and/or sensory system.

Decoding and disrupting left midfusiform gyrus activity during word reading

Significance A central issue in the neurobiology of reading is a debate regarding the visual representation of words, particularly in the left midfusiform gyrus (lmFG). Direct neural recordings, electrical brain stimulation, and pre-/postsurgical neuropsychological testing provided strong evidence that the lmFG supports an orthographically specific “visual word form” system that becomes specialized for the representation of orthographic knowledge. Machine learning elucidated the dynamic role lmFG plays with an early processing stage organized by orthographic similarity and a later stage supporting individuation of single words. The results suggest that there is a dynamic shift from gist-level to individuated orthographic representation in the lmFG in service of visual word recognition. The nature of the visual representation for words has been fiercely debated for over 150 y. We used direct brain stimulation, pre- and postsurgical behavioral measures, and intracranial electroencephalography to provide support for, and elaborate upon, the visual word form hypothesis. This hypothesis states that activity in the left midfusiform gyrus (lmFG) reflects visually organized information about words and word parts. In patients with electrodes placed directly in their lmFG, we found that disrupting lmFG activity through stimulation, and later surgical resection in one of the patients, led to impaired perception of whole words and letters. Furthermore, using machine-learning methods to analyze the electrophysiological data from these electrodes, we found that information contained in early lmFG activity was consistent with an orthographic similarity space. Finally, the lmFG contributed to at least two distinguishable stages of word processing, an early stage that reflects gist-level visual representation sensitive to orthographic statistics, and a later stage that reflects more precise representation sufficient for the individuation of orthographic word forms. These results provide strong support for the visual word form hypothesis and demonstrate that across time the lmFG is involved in multiple stages of orthographic representation.

The Influence of Nonremembered Affective Associations on Preference

An important influence on our preference toward a specific object is its associations with affective information. Here, the authors concentrate on the role of memory on shaping such preferences. Specifically, the authors used a multistage behavioral paradigm that fostered associations between neutral shapes and affective images. Participants that explicitly remembered these affective associations preferred neutral shapes associated with positive images. Counterintuitively, participants who could not explicitly remember the associations preferred neutral shapes that were associated with negative images. Generally, the difference in preference between participants who could and could not remember the affective associations demonstrates a critical link between memory and preference formation. The authors propose that the preference for negatively associated items is a manifestation of a mechanism that produces an inherent incentive for rapidly assessing potentially threatening aspects in the environment.

Movement-related dynamics of cortical oscillations in Parkinson’s disease and essential tremor

Recent electrocorticography data have demonstrated excessive coupling of beta-phase to gamma-amplitude in primary motor cortex and that deep brain stimulation facilitates motor improvement by decreasing baseline phase-amplitude coupling. However, both the dynamic modulation of phase-amplitude coupling during movement and the general cortical neurophysiology of other movement disorders, such as essential tremor, are relatively unexplored. To clarify the relationship of these interactions in cortical oscillatory activity to movement and disease state, we recorded local field potentials from hand sensorimotor cortex using subdural electrocorticography during a visually cued, incentivized handgrip task in subjects with Parkinsons disease (n = 11), with essential tremor (n = 9) and without a movement disorder (n = 6). We demonstrate that abnormal coupling of the phase of low frequency oscillations to the amplitude of gamma oscillations is not specific to Parkinsons disease, but also occurs in essential tremor, most prominently for the coupling of alpha to gamma oscillations. Movement kinematics were not significantly different between these groups, allowing us to show for the first time that robust alpha and beta desynchronization is a shared feature of sensorimotor cortical activity in Parkinsons disease and essential tremor, with the greatest high-beta desynchronization occurring in Parkinsons disease and the greatest alpha desynchronization occurring in essential tremor. We also show that the spatial extent of cortical phase-amplitude decoupling during movement is much greater in subjects with Parkinsons disease and essential tremor than in subjects without a movement disorder. These findings suggest that subjects with Parkinsons disease and essential tremor can produce movements that are kinematically similar to those of subjects without a movement disorder by reducing excess sensorimotor cortical phase-amplitude coupling that is characteristic of these diseases.